Elsevier

Scientia Horticulturae

Volume 303, 20 September 2022, 111239
Scientia Horticulturae

Metabolomic profiling and energy metabolism modulation unveil the mechanisms involved in enhanced disease resistance of postharvest broccoli by Meyerozyma guilliermondii

https://doi.org/10.1016/j.scienta.2022.111239Get rights and content

Highlights

  • M. guilliermondii decreased natural decay of postharvest broccoli.

  • Energy production and supply in broccoli were increased by M. guilliermondii.

  • M. guilliermondii significantly induced the synthesis of secondary metabolites.

  • Accumulation of sugar alcohols were enhanced by the yeast.

  • The levels of unsaturated fatty acids and intermediates, GSH were also increased.

Abstract

Postharvest diseases of broccoli resulted in quality deterioration and huge economic loss. This study investigated the biocontrol efficacy of Meyerozyma guilliermondii against natural decay of postharvest broccoli. Meanwhile, the mechanisms involved in the enhanced disease resistance of broccoli by M. guilliermondii were explored based on energy metabolism modulation and metabolomic analysis of broccoli. The results showed that M. guilliermondii could alleviate the disease index of postharvest broccoli. This yeast could potentially increase energy production and supply through inducing the activities of related enzymes and maintaining a higher ATP level. Metabolomic analysis illustrated that the treatment with M. guilliermondii significantly increased secondary metabolites synthesis, sugar alcohols accumulation, the level of unsaturated fatty acids and their metabolic intermediates, and glutathione level. In conclusion, M. guilliermondii improved the disease resistance of postharvest broccoli through enhancing energy production and supply, synthesis of resistant compounds, and thus reducing the natural decay disease index of broccoli.

Introduction

Broccoli (Brassica oleracea var. italic) is a globally consumed vegetable of Brassicaceae family. It is considered as a healthy vegetable and functional food due to the richness of diverse nutrients (minerals, vitamins, and dietary fiber etc.) and phytochemicals (glucosinolates and phenolic compounds etc.) (Li et al., 2022; Chen et al., 2022). Broccoli is a seasonal vegetable that needs to be stored for consumption throughout the year. However, vegetables of Brassicaceae family are susceptible to fungal species of the genus Alternaria which can cause leaf spot diseases (Reis and Boiteux, 2010; De Britto et al., 2020). Fusarium oxysporum Schlectend. Fr which is a fugal pathogen of numerous plant host species and agricultural crops, can also infect vegetables of Brassicaceae family (Rios et al., 2021). These fungal pathogens still lurk on the postharvest vegetables, and the spores would germinate under favorable conditions during storage, transportation and sale, thus causing the decay of host vegetables (Tournas, 2005). Additionally, due to the crisp and tender characteristics of vegetables of Brassicaceae family, they are also susceptible to the infection by other pathogens during storage and transportation, and thus causing huge economic losses (Guo et al., 2015). Therefore, it is necessary to take effective measures to control postharvest diseases of broccoli.

At present, the use of chemical fungicides is an effective measure to control postharvest diseases of vegetables. Due to the emergence of fungicide resistance in pathogens, the potentially hazardous effects of fungicide residues, and the negative effects on the environment, more eco-friendly and safer methods are driven to be developed for the management of postharvest diseases. Biological control using antagonistic yeast has achieved considerable attention and showed great potential in controlling postharvest diseases of fruits and vegetables for its sustainability, environmental friendliness and biosafety (Yu et al., 2020).

The previous reports indicated that the mechanisms by which yeast interacted with pathogens and host tissues mainly including competition for nutrients and space, mycoparasitism, secretion of antifungal substances, and induction of host resistance (Spadaro and Droby, 2016). Among them, induction of host resistance was the most complicated one and involved mitogen activated protein kinase signaling (MAPK), phytohormone signaling and downstream gene expression, and biosynthesis of resistant compounds etc. Omics techniques is a powerful tool to study the global effect of different treatments on the fruits and vegetables, and thus analyzing the mechanisms involved in the enhanced diseased resistance. Transcriptomic and/or proteomic technologies were widely used to study the effects of various treatments on the expression of genes and proteins in fruits and vegetables, and then bioinformatics analysis of the differentially expressed genes and proteins was performed to speculate the mechanisms involved in the improved disease resistance of fruits and vegetables. For example, a global view of the differentially expressed genes and proteins in grapes based on these two omics techniques unveiled the mechanisms involved in the enhanced disease resistance of grapes by Yarrowia lipolytic (Zhao et al., 2021). The improvement of disease resistance of fruits and vegetables is also closely related to the synthesis of some resistant substances, such as unsaturated fatty acids (Kachroo and Kachroo, 2009) and secondary metabolites (Tuladhar et al., 2021; Toffolatti et al., 2021; Thippeswamy et al., 2021) etc. Metabolomics is used to identify a mass of compounds with diverse physical and chemical characteristics in a system or organism mainly by the analytical technologies of nuclear magnetic resonance (NMR) and mass spectrometry (MS), and possibly performed by new technology of ion mobility separation (IMS) in the future to provide a new dimension for chromatography and MS (Li et al., 2021). It can reflect the globally dynamic change of metabolites under given conditions (Chen et al., 2020). Metabolomics has been widely used in the fields of food and agriculture, such as food quality and safety, multifaceted defense response of plants etc. It has been reported that metabolomics was used to investigate the metabolic changes of mung bean during its germination and sprouting process under different energy status, which was useful for improving its quality through controlling the development process (Chen et al., 2019). In the previous study, global metabolomic profiling involved in the improved disease resistance of citrus fruit by Rhodosporidium paludigenum were performed based on comparative metabolomics (Lu et al., 2015). However, the application of metabolomics in studying defense response of fruits and vegetables is far less extensive than other omics, and there is a wide developing space in exploring the mechanisms involved the induced diseased resistance of fruits and vegetables through metabolomic analysis.

Up to now, the researches on controlling postharvest diseases of broccoli by antagonistic yeast is limited, and the involved mechanisms are not clear, which has great potential and prospect for studying. Controlling the postharvest disease of broccoli by antagonistic yeast and unravelling the mechanisms involved in the enhanced disease resistance were critically important to improve its quality in global markets with reduced use of chemical fungicides. M. guilliermondii showed great potential in controlling postharvest diseases of fruits such as pears, apples and mandarin fruits (Yan et al., 2018; Huang et al., 2021; Wang et al., 2021). In the present study, the yeast Meyerozyma guilliermondii screened by our research team was used for postharvest disease management of broccoli, energy metabolism modulation were investigated and metabolomic technology was employed to illustrate the mechanisms involved in disease resistance of broccoli enhanced by M. guilliermondii.

Section snippets

Yeast

M. guilliermondii was screened by our research team and preserved in China Center for Type Culture Collection with the accession number CCTCC M2019933. It was cultured in nutrient yeast dextrose broth (NYDB, containing 8 g of nutrient broth, 10 g of glucose, 5 g of yeast extract, 1 L of distilled water) at 180 rpm and 28 °C for 24 h. Then the cells were collected by centrifugation at 8000 × g for 10 min and washed with sterile saline twice. After that, the cell concentration was adjusted to

Control efficacy of M. guilliermondii against natural decay of postharvest broccoli

Fig. 1 showed that the disease index of broccoli treated with M. guilliermondii were significantly lower than that of the control group after storage for 3 and 5 d (P < 0.05), indicating that this antagonistic yeast had a good control efficacy against natural decay of postharvest broccoli.

Effects of M. guilliermondii on activities of enzymes related to energy metabolism in broccoli

SDH activity can generally be used as an indicator to evaluate the operation degree of TCA cycle, and this enzyme also participates in oxidative phosphorylation. As shown in Fig. 2A, SDH activity in M.

Discussion

Broccoli is a seasonal and globally consumed vegetable. Postharvest diseases are an important limiting factor for its supply chain including storage, transportation and sale. Biological control of postharvest diseases of fruits and vegetables using antagonistic yeast has achieved considerable attention for its sustainability, environmental friendliness and biosafety. However, there are few studies on controlling postharvest diseases of broccoli by antagonistic yeast. In this study, M.

Conclusions

In summary, the disease resistance of postharvest broccoli was improved through enhancing the energy production and supply for various life activities, biosynthesis of secondary metabolites, sugar alcohols accumulation, the level of unsaturated fatty acids and important intermediates, and GSH level when it interacted with M. guilliermondii, and thus resulting in alleviated disease index. The observations of this study unraveled the regulation of energy metabolism and the significantly regulated

CRediT authorship contribution statement

Xiaoyun Zhang: Project administration, Methodology, Writing – original draft. Hongyao Zhou: Data curation, Writing – original draft. Yuqi Yao: Methodology, Investigation. Junyi Wang: Data curation, Methodology. Xiangyu Gu: Methodology. Bo Li: Writing – review & editing. Lina Zhao: Data curation. Hongyin Zhang: Supervision, Conceptualization, Writing – review & editing, Funding acquisition.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (No. 32072276).

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